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Functional Diversity of Resilin in Arthropoda

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Functional Diversity of Resilin in Arthropoda Functional diversity of resilin in Arthropoda Jan Michels*, Esther Appel and Stanislav N. Gorb Review Open Access Address: Beilstein J. Nanotechnol. 2016, 7, 1241–1259. Department of Functional Morphology and Biomechanics, Institute of doi:10.3762/bjnano.7.115 Zoology, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1–9, D-24118 Kiel, Germany Received: 18 April 2016 Accepted: 15 July 2016 Email: Published: 01 September 2016 Jan Michels* - [email protected] This article is part of the Thematic Series "Biological and biomimetic * Corresponding author materials and surfaces". Keywords: Associate Editor: K. Koch biological materials; biomechanics; composites; elastomeric proteins; functional morphology © 2016 Michels et al.; licensee Beilstein-Institut. License and terms: see end of document. Abstract Resilin is an elastomeric protein typically occurring in exoskeletons of arthropods. It is composed of randomly orientated coiled polypeptide chains that are covalently cross-linked together at regular intervals by the two unusual amino acids dityrosine and trityrosine forming a stable network with a high degree of flexibility and mobility. As a result of its molecular prerequisites, resilin features exceptional rubber-like properties including a relatively low stiffness, a rather pronounced long-range deformability and a nearly perfect elastic recovery. Within the exoskeleton structures, resilin commonly forms composites together with other proteins and/or chitin fibres. In the last decades, numerous exoskeleton structures with large proportions of resilin and various resilin func- tions have been described. Today, resilin is known to be responsible for the generation of deformability and flexibility in mem- brane and joint systems, the storage of elastic energy in jumping and catapulting systems, the enhancement of adaptability to uneven surfaces in attachment and prey catching systems, the reduction of fatigue and damage in reproductive, folding and feeding systems and the sealing of wounds in a traumatic reproductive system. In addition, resilin is present in many compound eye lenses and is suggested to be a very suitable material for optical elements because of its transparency and amorphousness. The evolution of this remarkable functional diversity can be assumed to have only been possible because resilin exhibits a unique combination of dif- ferent outstanding properties. Review Resilin – the pliant protein Elastomeric proteins occur in a large range of organisms and bi- abductin of bivalve molluscs and gluten of wheat [1]. Besides ological structures, and the spectrum of their biological func- spider silk proteins, resilin is certainly the best-known among tions is very broad [1]. They feature a great diversity including the elastomeric proteins existing in arthropods. The first de- well-known examples such as elastin, titin and fibrillin present scription of resilin, which has often been called rubber-like pro- in vertebrate muscles and connective tissues, byssus and tein, was based on analyses of three different insect exoskel- 1241 Beilstein J. Nanotechnol. 2016, 7, 1241–1259. eton elements: the wing hinge and the prealar arm of the desert the fully cross-linked protein is called resilin, whereas the not locust (Schistocerca gregaria) (also described for the migratory yet cross-linked or not fully cross-linked protein is called pro- locust (Locusta migratoria), Figure 1A,B) and the so-called resilin [6]. Within hydrolysates of resilin, glycine constitutes the elastic tendon of the pleuro-subalar muscles in dragonflies of largest proportion (30–40%) of the total residues [7,8]. Such the genus Aeshna [2]. Additional insights into the character- hydrolysates also feature the two unusual amino acids dityr- istics of resilin that had been gained shortly after this descrip- osine and trityrosine, which were identified to form the cross- tion [3,4] resulted in a comprehensive compilation of the then links between the polypeptide chains [9]. existing knowledge of resilin properties [5]. Resilin consists of a network of randomly orientated coiled polypeptide chains that The mechanical properties of resilin strongly depend on the have a high degree of flexibility and mobility and are linked degree of hydration because resilin is plasticised by water [5]. together at regular intervals by stable covalent cross-links. Only When resilin is completely hydrated, it behaves close to a Figure 1: Occurrence of resilin in insects and crustaceans. Confocal laser scanning micrographs showing a wing hinge (A) and a prealar arm (B) of the migratory locust (Locusta migratoria), a wing vein joint of the common darter (Sympetrum striolatum) (C) and the ventral side of a female copepod of the species Temora longicornis (D). (A–C) Overlays of four different autofluorescences exhibited by the exoskeleton. Blue colours indicate large proportions of resilin, while green structures consist mainly of non- or weakly-sclerotised chitinous material, and red structures are composed of rela- tively strongly sclerotised chitinous structures. (D) Blue = autofluorescence of resilin, red = Congo red fluorescence of stained chitinous exoskeleton parts, green = mixture of autofluorescence and Congo red fluorescence of stained chitinous exoskeleton parts. (A, C, D) Maximum intensity projec- tions. (B) Optical section. Scale bars = 100 µm (A, B), 20 µm (C), 200 µm (D). (A–D) Adapted with permission from [10], copyright 2011 John Wiley and Sons. 1242 Beilstein J. Nanotechnol. 2016, 7, 1241–1259. perfect rubber [3,4,11]. Due to its molecular prerequisites, In order to allow a classification of exoskeleton structures as resilin then exhibits a near-perfect resilience of up to 92–97% resilin-containing exoskeleton according to the definition of and a fatigue limit of over 300 million cycles [12]. With respect Andersen and Weis-Fogh [5], these structures must conform to to resilience, resilin is unmatched by any other elastomeric pro- the wing hinge, the prealar arm and the elastic tendon tein and the best synthetic rubbers such as unfilled poly- mentioned above with respect to their properties, which can be butadiene [13,14]. Fully hydrated resilin has a rather low stiff- tested with a number of methods [5]. Resilin is colourless, ness. In the elastic tendons of dragonflies and locust ligaments transparent and amorphous. Accordingly, structures with very mentioned above, it was found to have a Young’s modulus of large resilin proportions can be easily distinguished from struc- 0.6–0.7 MPa and 0.9 MPa, respectively [11]. In addition, fully tures with relatively large proportions of chitin that are typical- hydrated resilin can be stretched to more than three times its ly pigmented and only slightly transparent or sometimes, when original length and compressed to one third of its original the sclerotisation is very pronounced, not transparent at all. length, and when the tensile and compressive forces are re- When immersed in aqueous media and in many anhydrous leased, resilin goes back to its initial state without having any hydrophilic liquids, resilin exhibits an isotropic swelling, which residual deformations [3,4,13]. is reversible and depends on the pH. (It is least pronounced at pH values of about 4.) In its hydrated state, resilin is swollen Until today, resilin has been found to exist mainly in insect and features its typical rubbery nature, long-range deformab- exoskeleton structures where this protein has a number of ility and complete elastic recovery. Furthermore, if hydrated different functions, which include (1) the storage of elastic resilin is tensioned, it will become birefringent, and the birefrin- energy in jumping systems [15-20], (2) the reduction of fatigue gence will be positive in the direction of the extension. When in folding wings of beetles and dermapterans [21,22], (3) resilin is completely dried, it loses its rubber-like character- the enhancement of the adaptability of attachment pads to istics and becomes relatively hard and brittle. Proteolytic en- uneven surfaces [23] and (4) the generation of flexibility of zymes such as pepsin or trypsin can be applied to test for the wing vein joints in dragonflies and damselflies [24-26]. Resilin presence and distribution of resilin, because resilin is known to has also been reported to be present in the exoskeletons of other be digested by such enzymes. Resilin has been shown to be arthropod taxa such as crustaceans [10,27-30] (Figure 1D), stained by single conventional dyes. Chemical reactions with scorpions [31] and centipedes [32]. In addition, resilin-like pro- the Masson and Mallory dyes were mentioned to stain resilin teins that contain dityrosine and trityrosine are known to exist in red. Staining of resilin with aqueous solutions of methylene several non-arthropod taxa including monogeneans [33,34], blue and toluidine blue is a common method and can provide nematodes [35], mussels [36] and sea urchins [37] indicating good information about the presence and distribution of resilin. that resilin likely originated much earlier in the evolution of When resilin is stained with one of these two dyes, it does not invertebrates than previously assumed. show metachromasia. Among the amino acids that form resilin, dityrosine and trityrosine exhibit a relatively pronounced auto- The properties of resilin-containing exoskeletons can strongly fluorescence. This autofluorescence is present in natural resilin- differ between structures and organisms. The reason is that in containing
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